1932

Abstract

DNA origami enables the bottom-up construction of chemically addressable, nanoscale objects with user-defined shapes and tailored functionalities. As such, not only can DNA origami objects be used to improve existing experimental methods in biophysics, but they also open up completely new avenues of exploration. In this review, we discuss basic biophysical concepts that are relevant for prospective DNA origami users. We summarize biochemical strategies for interfacing DNA origami with biomolecules of interest. We describe various applications of DNA origami, emphasizing the added value or new biophysical insights that can be generated: rulers and positioning devices, force measurement and force application devices, alignment supports for structural analysis for biomolecules in cryogenic electron microscopy and nuclear magnetic resonance, probes for manipulating and interacting with lipid membranes, and programmable nanopores. We conclude with some thoughts on so-far little explored opportunities for using DNA origami in more complex environments such as the cell or even organisms.

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2021-05-06
2024-04-24
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Literature Cited

  1. 1. 
    Aghebat Rafat A, Sagredo S, Thalhammer M, Simmel FC 2020. Barcoded DNA origami structures for multiplexed optimization and enrichment of DNA-based protein-binding cavities. Nat. Chem. 12:852–59
    [Google Scholar]
  2. 2. 
    Aksel T, Yu Z, Cheng Y, Douglas SM. 2021. Molecular goniometers for single-particle cryo-electron microscopy of DNA-binding proteins. Nat. Biotechnol. 39:37886
    [Google Scholar]
  3. 3. 
    Bai X, Martin TG, Scheres SHW, Dietz H 2012. Cryo-EM structure of a 3D DNA-origami object. PNAS 109:20012–17
    [Google Scholar]
  4. 4. 
    Bastings MMC, Anastassacos FM, Ponnuswamy N, Leifer FG, Cuneo G et al. 2018. Modulation of the cellular uptake of DNA origami through control over mass and shape. Nano Lett 18:3557–64
    [Google Scholar]
  5. 5. 
    Bednar J, Furrer P, Katritch V, Stasiak AZ, Dubochet J, Stasiak A. 1995. Determination of DNA persistence length by cryo-electron microscopy: separation of the static and dynamic contributions to the apparent persistence length of DNA. J. Mol. Biol. 254:579–94
    [Google Scholar]
  6. 6. 
    Bell NAW, Engst CR, Ablay M, Divitini G, Ducati C et al. 2012. DNA origami nanopores. Nano Lett 12:512–17
    [Google Scholar]
  7. 7. 
    Bellot G, McClintock MA, Chou JJ, Shih WM. 2013. DNA nanotubes for NMR structure determination of membrane proteins. Nat. Protoc. 8:755–70
    [Google Scholar]
  8. 8. 
    Berardi MJ, Shih WM, Harrison SC, Chou JJ. 2011. Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 476:109–13
    [Google Scholar]
  9. 9. 
    Bian X, Zhang Z, Xiong Q, De Camilli P, Lin C 2019. A programmable DNA-origami platform for studying lipid transfer between bilayers. Nat. Chem. Biol. 15:830–37
    [Google Scholar]
  10. 10. 
    Boutureira O, Bernardes GJL. 2015. Advances in chemical protein modification. Chem. Rev. 115:2174–95
    [Google Scholar]
  11. 11. 
    Bustamante C, Marko JF, Siggia ED, Smith S. 1994. Entropic elasticity of lambda-phage DNA. Science 265:1599–600
    [Google Scholar]
  12. 12. 
    Czogalla A, Kauert DJ, Franquelim HG, Uzunova V, Zhang Y et al. 2015. Amphipathic DNA origami nanoparticles to scaffold and deform lipid membrane vesicles. Angew. Chem. 54:6501–5
    [Google Scholar]
  13. 13. 
    Dekker C. 2007. Solid-state nanopores. Nat. Nanotechnol. 2:209–15
    [Google Scholar]
  14. 14. 
    Dietz H, Berkemeier F, Bertz M, Rief M 2006. Anisotropic deformation response of single protein molecules. PNAS 103:12724–28
    [Google Scholar]
  15. 15. 
    Dietz H, Douglas SM, Shih WM. 2009. Folding DNA into twisted and curved nanoscale shapes. Science 325:725–30
    [Google Scholar]
  16. 16. 
    Dietz H, Rief M 2006. Protein structure by mechanical triangulation. PNAS 103:1244–47
    [Google Scholar]
  17. 17. 
    Dong Y, Chen S, Zhang S, Sodroski J, Yang Z et al. 2018. Folding DNA into a lipid-conjugated nanobarrel for controlled reconstitution of membrane proteins. Angew. Chem. 57:2072–76
    [Google Scholar]
  18. 18. 
    Douglas SM, Bachelet I, Church GM. 2012. A logic-gated nanorobot for targeted transport of molecular payloads. Science 335:831–34
    [Google Scholar]
  19. 19. 
    Douglas SM, Chou JJ, Shih WM 2007. DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. PNAS 104:6644–48
    [Google Scholar]
  20. 20. 
    Dutta PK, Zhang Y, Blanchard AT, Ge C, Rushdi M et al. 2018. Programmable multivalent DNA-origami tension probes for reporting cellular traction forces. Nano Lett 18:4803–11
    [Google Scholar]
  21. 21. 
    Endo M, Katsuda Y, Hidaka K, Sugiyama H. 2010. A versatile DNA nanochip for direct analysis of DNA base-excision repair. Angew. Chem. 49:9412–16
    [Google Scholar]
  22. 22. 
    Engelhardt FAS, Praetorius F, Wachauf CH, Brüggenthies G, Kohler F et al. 2019. Custom-size, functional, and durable DNA origami with design-specific scaffolds. ACS Nano 13:5015–27
    [Google Scholar]
  23. 23. 
    Evans E, Ritchie K 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541–55
    [Google Scholar]
  24. 24. 
    Florin EL, Moy VT, Gaub HE. 1994. Adhesion forces between individual ligand-receptor pairs. Science 264:415–17
    [Google Scholar]
  25. 25. 
    Franquelim HG, Dietz H, Schwille P. 2021. Reversible membrane deformations by straight DNA origami filaments. Soft Matter 17:27687
    [Google Scholar]
  26. 26. 
    Franquelim HG, Khmelinskaia A, Sobczak J-P, Dietz H, Schwille P. 2018. Membrane sculpting by curved DNA origami scaffolds. Nat. Commun. 9:811
    [Google Scholar]
  27. 27. 
    Fu J, Liu M, Liu Y, Woodbury NW, Yan H. 2012. Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures. J. Am. Chem. Soc. 134:5516–19
    [Google Scholar]
  28. 28. 
    Funke JJ, Dietz H. 2016. Placing molecules with Bohr radius resolution using DNA origami. Nat. Nanotechnol. 11:47–52
    [Google Scholar]
  29. 29. 
    Funke JJ, Ketterer P, Lieleg C, Korber P, Dietz H. 2016. Exploring nucleosome unwrapping using DNA origami. Nano Lett 16:7891–98
    [Google Scholar]
  30. 30. 
    Funke JJ, Ketterer P, Lieleg C, Schunter S, Korber P, Dietz H. 2016. Uncovering the forces between nucleosomes using DNA origami. Sci. Adv. 2:e1600974
    [Google Scholar]
  31. 31. 
    Gautier A, Juillerat A, Heinis C, Reis Corrêa I Jr., Kindermann M et al. 2008. An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15:128–36
    [Google Scholar]
  32. 32. 
    Gerling T, Kube M, Kick B, Dietz H. 2018. Sequence-programmable covalent bonding of designed DNA assemblies. Sci. Adv. 4:eaau1157
    [Google Scholar]
  33. 33. 
    Good MC, Zalatan JG, Lim WA. 2011. Scaffold proteins: hubs for controlling the flow of cellular information. Science 332:680–86
    [Google Scholar]
  34. 34. 
    Göpfrich K, Li C-Y, Ricci M, Bhamidimarri SP, Yoo J et al. 2016. Large-conductance transmembrane porin made from DNA origami. ACS Nano 10:8207–14
    [Google Scholar]
  35. 35. 
    Grabarek Z, Gergely J. 1990. Zero-length crosslinking procedure with the use of active esters. Anal. Biochem. 185:131–35
    [Google Scholar]
  36. 36. 
    Greenleaf WJ, Woodside MT, Block SM. 2007. High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct. 36:171–90
    [Google Scholar]
  37. 37. 
    Grome MW, Zhang Z, Pincet F, Lin C. 2018. Vesicle tabulation with self-assembling DNA nanosprings. Angew. Chem. 57:5330–34
    [Google Scholar]
  38. 38. 
    Halvorsen K, Schaak D, Wong WP. 2011. Nanoengineering a single-molecule mechanical switch using DNA self-assembly. Nanotechnology 22:494005
    [Google Scholar]
  39. 39. 
    Henzler-Wildman K, Kern D. 2007. Dynamic personalities of proteins. Nature 450:964–72
    [Google Scholar]
  40. 40. 
    Hernández-Ainsa S, Bell NAW, Thacker VV, Göpfrich K, Misiunas K et al. 2013. DNA origami nanopores for controlling DNA translocation. ACS Nano 7:6024–30
    [Google Scholar]
  41. 41. 
    Hernández-Ainsa S, Misiunas K, Thacker VV, Hemmig EA, Keyser UF. 2014. Voltage-dependent properties of DNA origami nanopores. Nano Lett 14:1270–74
    [Google Scholar]
  42. 42. 
    Hong F, Zhang F, Liu Y, Yan H. 2017. DNA origami: scaffolds for creating higher order structures. Chem. Rev. 117:12584–640
    [Google Scholar]
  43. 43. 
    Huang C-M, Kucinic A, Johnson JA, Su H-J, Castro CE. 2020. Integrating computer-aided engineering and computer-aided design for DNA assemblies. bioRxiv 119701. https://doi.org/10.1101/2020.05.28.119701
    [Crossref]
  44. 44. 
    Iwaki M, Wickham SF, Ikezaki K, Yanagida T, Shih WM. 2016. A programmable DNA origami nanospring that reveals force-induced adjacent binding of myosin VI heads. Nat. Commun. 7:13715
    [Google Scholar]
  45. 45. 
    Jain M, Olsen HE, Paten B, Akeson M. 2016. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol 17:239
    [Google Scholar]
  46. 46. 
    Journot CMA, Ramakrishna V, Wallace MI, Turberfield AJ. 2019. Modifying membrane morphology and interactions with DNA origami clathrin-mimic networks. ACS Nano 13:9973–79
    [Google Scholar]
  47. 47. 
    Jungmann R, Steinhauer C, Scheible M, Kuzyk A, Tinnefeld P, Simmel FC. 2010. Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. Nano Lett 10:4756–61
    [Google Scholar]
  48. 48. 
    Junker JP, Ziegler F, Rief M. 2009. Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science 323:633–37
    [Google Scholar]
  49. 49. 
    Ke Y, Meyer T, Shih WM, Bellot G. 2016. Regulation at a distance of biomolecular interactions using a DNA origami nanoactuator. Nat. Commun. 7:10935
    [Google Scholar]
  50. 50. 
    Ketterer P, Willner EM, Dietz H. 2016. Nanoscale rotary apparatus formed from tight-fitting 3D DNA components. Sci. Adv. 2:e1501209
    [Google Scholar]
  51. 51. 
    Kilchherr F, Wachauf C, Pelz B, Rief M, Zacharias M, Dietz H. 2016. Single-molecule dissection of stacking forces in DNA. Science 353:aaf5508
    [Google Scholar]
  52. 52. 
    Kim J, Zhang C-Z, Zhang X, Springer TA. 2010. A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 466:992–95
    [Google Scholar]
  53. 53. 
    Kocabey S, Kempter S, List J, Xing Y, Bae W et al. 2015. Membrane-assisted growth of DNA origami nanostructure arrays. ACS Nano 9:3530–39
    [Google Scholar]
  54. 54. 
    Kopperger E, List J, Madhira S, Rothfischer F, Lamb DC, Simmel FC. 2018. A self-assembled nanoscale robotic arm controlled by electric fields. Science 359:296–301
    [Google Scholar]
  55. 55. 
    Kosuri P, Altheimer BD, Dai M, Yin P, Zhuang X. 2019. Rotation tracking of genome-processing enzymes using DNA origami rotors. Nature 572:136–40
    [Google Scholar]
  56. 56. 
    Kramm K, Schröder T, Gouge J, Vera AM, Gupta K et al. 2020. DNA origami-based single-molecule force spectroscopy elucidates RNA polymerase III pre-initiation complex stability. Nat. Commun. 11:2828
    [Google Scholar]
  57. 57. 
    Krishnan S, Ziegler D, Arnaut V, Martin TG, Kapsner K et al. 2016. Molecular transport through large-diameter DNA nanopores. Nat. Commun. 7:12787
    [Google Scholar]
  58. 58. 
    Langecker M, Arnaut V, Martin TG, List J, Renner S et al. 2012. Synthetic lipid membrane channels formed by designed DNA nanostructures. Science 338:932–36
    [Google Scholar]
  59. 59. 
    Le JV, Luo Y, Darcy MA, Lucas CR, Goodwin MF et al. 2016. Probing nucleosome stability with a DNA origami nanocaliper. ACS Nano 10:7073–84
    [Google Scholar]
  60. 60. 
    Lee DS, Qian H, Tay CY, Leong DT. 2016. Cellular processing and destinies of artificial DNA nanostructures. Chem. Soc. Rev. 45:4199–225
    [Google Scholar]
  61. 61. 
    Lin C, Jungmann R, Leifer AM, Li C, Levner D et al. 2012. Submicrometre geometrically encoded fluorescent barcodes self-assembled from DNA. Nat. Chem. 4:832–39
    [Google Scholar]
  62. 62. 
    Linko V, Eerikäinen M, Kostiainen MA. 2015. A modular DNA origami-based enzyme cascade nanoreactor. Chem. Commun. 51:5351–54
    [Google Scholar]
  63. 63. 
    List J, Falgenhauer E, Kopperger E, Pardatscher G, Simmel FC. 2016. Long-range movement of large mechanically interlocked DNA nanostructures. Nat. Commun. 7:12414
    [Google Scholar]
  64. 64. 
    Liu CC, Schultz PG. 2010. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79:413–44
    [Google Scholar]
  65. 65. 
    Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N et al. 2008. HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem. Biol. 3:373–82
    [Google Scholar]
  66. 66. 
    Mao H, Hart SA, Schink A, Pollok BA. 2004. Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc. 126:2670–71
    [Google Scholar]
  67. 67. 
    Martin TG, Bharat TAM, Joerger AC, Bai X, Praetorius F et al. 2016. Design of a molecular support for cryo-EM structure determination. PNAS 113:E7456–63
    [Google Scholar]
  68. 68. 
    Milczek EM. 2018. Commercial applications for enzyme-mediated protein conjugation: new developments in enzymatic processes to deliver functionalized proteins on the commercial scale. Chem. Rev. 118:119–41
    [Google Scholar]
  69. 69. 
    Moy VT, Florin EL, Gaub HE. 1994. Intermolecular forces and energies between ligands and receptors. Science 266:257–59
    [Google Scholar]
  70. 70. 
    Nickels PC, Wünsch B, Holzmeister P, Bae W, Kneer LM et al. 2016. Molecular force spectroscopy with a DNA origami-based nanoscopic force clamp. Science 354:305–7
    [Google Scholar]
  71. 71. 
    Niemeyer CM. 2002. The developments of semisynthetic DNA-protein conjugates. Trends Biotechnol 20:395–401
    [Google Scholar]
  72. 72. 
    Niemeyer CM. 2010. Semisynthetic DNA-protein conjugates for biosensing and nanofabrication. Angew. Chem. 49:1200–16
    [Google Scholar]
  73. 73. 
    Niemeyer CM, Sano T, Smith CL, Cantor CR. 1994. Oligonucleotide-directed self-assembly of proteins: semisynthetic DNA–streptavidin hybrid molecules as connectors for the generation of macroscopic arrays and the construction of supramolecular bioconjugates. Nucleic Acids Res 22:5530–39
    [Google Scholar]
  74. 74. 
    Noji H, Yasuda R, Yoshida M, Kinosita K Jr. 1997. Direct observation of the rotation of F1-ATPase. Nature 386:299–302
    [Google Scholar]
  75. 75. 
    Pawson T, Scott JD. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075–80
    [Google Scholar]
  76. 76. 
    Perrault SD, Shih WM. 2014. Virus-inspired membrane encapsulation of DNA nanostructures to achieve in vivo stability. ACS Nano 8:5132–40
    [Google Scholar]
  77. 77. 
    Pfitzner E, Wachauf C, Kilchherr F, Pelz B, Shih WM et al. 2013. Rigid DNA beams for high-resolution single-molecule mechanics. Angew. Chem. 52:7766–71
    [Google Scholar]
  78. 78. 
    Phillips R, Kondev J, Theriot J. 2013. Physical Biology of the Cell New York: Garland Sci.
  79. 79. 
    Plesa C, Ananth AN, Linko V, Gülcher C, Katan AJ et al. 2014. Ionic permeability and mechanical properties of DNA origami nanoplates on solid-state nanopores. ACS Nano 8:35–43
    [Google Scholar]
  80. 80. 
    Ponnuswamy N, Bastings MMC, Nathwani B, Ryu JH, Chou LYT et al. 2017. Oligolysine-based coating protects DNA nanostructures from low-salt denaturation and nuclease degradation. Nat. Commun. 8:15654
    [Google Scholar]
  81. 81. 
    Praetorius F, Kick B, Behler KL, Honemann MN, Weuster-Botz D, Dietz H. 2017. Biotechnological mass production of DNA origami. Nature 552:84–87
    [Google Scholar]
  82. 82. 
    Rabuka D, Rush JS, deHart GW, Wu P, Bertozzi CR. 2012. Site-specific chemical protein conjugation using genetically encoded aldehyde tags. Nat. Protoc. 7:1052–67
    [Google Scholar]
  83. 83. 
    Ramezani H, Dietz H. 2020. Building machines with DNA molecules. Nat. Rev. Genet. 21:5–26
    [Google Scholar]
  84. 84. 
    Rand AC, Jain M, Eizenga JM, Musselman-Brown A, Olsen HE et al. 2017. Mapping DNA methylation with high-throughput nanopore sequencing. Nat. Methods 14:411–13
    [Google Scholar]
  85. 85. 
    Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109–12
    [Google Scholar]
  86. 86. 
    Rinker S, Ke Y, Liu Y, Chhabra R, Yan H. 2008. Self-assembled DNA nanostructures for distance dependent multivalent ligand-protein binding. Nat. Nanotechnol. 3:418–22
    [Google Scholar]
  87. 87. 
    Rosen CB, Kodal ALB, Nielsen JS, Schaffert DH, Scavenius C et al. 2014. Template-directed covalent conjugation of DNA to native antibodies, transferrin and other metal-binding proteins. Nat. Chem. 6:804–9
    [Google Scholar]
  88. 88. 
    Rosier BJHM, Cremers GAO, Engelen W, Merkx M, Brunsveld L, de Greef TFA. 2017. Incorporation of native antibodies and Fc-fusion proteins on DNA nanostructures via a modular conjugation strategy. Chem. Commun. 53:7393–96
    [Google Scholar]
  89. 89. 
    Rosier BJHM, Markvoort AJ, Gumí Audenis B, Roodhuizen JAL, den Hamer A et al. 2020. Proximity-induced caspase-9 activation on a DNA origami-based synthetic apoptosome. Nat. Catal. 3:295–306
    [Google Scholar]
  90. 90. 
    Rothemund PWK. 2006. Folding DNA to create nanoscale shapes and patterns. Nature 440:297–302
    [Google Scholar]
  91. 91. 
    Sannohe Y, Endo M, Katsuda Y, Hidaka K, Sugiyama H. 2010. Visualization of dynamic conformational switching of the G-quadruplex in a DNA nanostructure. J. Am. Chem. Soc. 132:16311–13
    [Google Scholar]
  92. 92. 
    Schmied JJ, Gietl A, Holzmeister P, Forthmann C, Steinhauer C et al. 2012. Fluorescence and super-resolution standards based on DNA origami. Nat. Methods 9:1133–34
    [Google Scholar]
  93. 93. 
    Selvin PR, Ha T. 2008. Single-Molecule Techniques: A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
  94. 94. 
    Shaw A, Hoffecker IT, Smyrlaki I, Rosa J, Grevys A et al. 2019. Binding to nanopatterned antigens is dominated by the spatial tolerance of antibodies. Nat. Nanotechnol. 14:184–90
    [Google Scholar]
  95. 95. 
    Simpson JT, Workman RE, Zuzarte PC, David M, Dursi LJ, Timp W. 2017. Detecting DNA cytosine methylation using nanopore sequencing. Nat. Methods 14:407–10
    [Google Scholar]
  96. 96. 
    Singh Y, Murat P, Defrancq E. 2010. Recent developments in oligonucleotide conjugation. Chem. Soc. Rev. 39:2054–70
    [Google Scholar]
  97. 97. 
    Steinhauer C, Jungmann R, Sobey TL, Simmel FC, Tinnefeld P. 2009. DNA origami as a nanoscopic ruler for super-resolution microscopy. Angew. Chem. 48:8870–73
    [Google Scholar]
  98. 98. 
    Stigler J, Ziegler F, Gieseke A, Gebhardt JC, Rief M. 2011. The complex folding network of single calmodulin molecules. Science 334:512–16
    [Google Scholar]
  99. 99. 
    Šulc P, Romano F, Ouldridge TE, Rovigatti L, Doye JPK, Louis AA. 2012. Sequence-dependent thermodynamics of a coarse-grained DNA model. J. Chem. Phys. 137:135101
    [Google Scholar]
  100. 100. 
    Suzuki Y, Endo M, Canas C, Ayora S, Alonso JC et al. 2014. Direct analysis of Holliday junction resolving enzyme in a DNA origami nanostructure. Nucleic Acids Res 42:7421–28
    [Google Scholar]
  101. 101. 
    Suzuki Y, Endo M, Sugiyama H. 2015. Lipid-bilayer-assisted two-dimensional self-assembly of DNA origami nanostructures. Nat. Commun. 6:8052
    [Google Scholar]
  102. 102. 
    Thomsen RP, Malle MG, Okholm AH, Krishnan S, Bohr SS-R et al. 2019. A large size-selective DNA nanopore with sensing applications. Nat. Commun. 10:5655
    [Google Scholar]
  103. 103. 
    Tinland B, Pluen A, Sturm J, Weill G. 1997. Persistence length of single-stranded DNA. Macromolecules 30:5763–65
    [Google Scholar]
  104. 104. 
    Trads JB, Tørring T, Gothelf KV. 2017. Site-selective conjugation of native proteins with DNA. Acc. Chem. Res. 50:1367–74
    [Google Scholar]
  105. 105. 
    Veneziano R, Moyer TJ, Stone MB, Wamhoff E-C, Read BJ et al. 2020. Role of nanoscale antigen organization on B-cell activation probed using DNA origami. Nat. Nanotechnol. 15:716–23
    [Google Scholar]
  106. 106. 
    Wagenbauer KF, Engelhardt FAS, Stahl E, Hechtl VK, Stömmer P et al. 2017. How we make DNA origami. ChemBioChem 18:1873–85
    [Google Scholar]
  107. 107. 
    Wamhoff E-C, Banal JL, Bricker WP, Shepherd TR, Parsons MF et al. 2019. Programming structured DNA assemblies to probe biophysical processes. Annu. Rev. Biophys. 48:395–419
    [Google Scholar]
  108. 108. 
    Wang P, Rahman MA, Zhao Z, Weiss K, Zhang C et al. 2018. Visualization of the cellular uptake and trafficking of DNA origami nanostructures in cancer cells. J. Am. Chem. Soc. 140:2478–84
    [Google Scholar]
  109. 109. 
    Wei R, Martin TG, Rant U, Dietz H. 2012. DNA origami gatekeepers for solid-state nanopores. Angew. Chem. 51:4864–67
    [Google Scholar]
  110. 110. 
    Wells JA, McClendon CL. 2007. Reaching for high-hanging fruit in drug discovery at protein–protein interfaces. Nature 450:1001–9
    [Google Scholar]
  111. 111. 
    Wilner OI, Weizmann Y, Gill R, Lioubashevski O, Freeman R, Willner I. 2009. Enzyme cascades activated on topologically programmed DNA scaffolds. Nat. Nanotechnol. 4:249–54
    [Google Scholar]
  112. 112. 
    Xu W, Nathwani B, Lin C, Wang J, Karatekin E et al. 2016. A programmable DNA origami platform to organize SNAREs for membrane fusion. J. Am. Chem. Soc. 138:4439–47
    [Google Scholar]
  113. 113. 
    Yang Y, Wang J, Shigematsu H, Xu W, Shih WM et al. 2016. Self-assembly of size-controlled liposomes on DNA nanotemplates. Nat. Chem. 8:476–83
    [Google Scholar]
  114. 114. 
    Zhang P, Liu X, Liu P, Wang F, Ariyama H et al. 2020. Capturing transient antibody conformations with DNA origami epitopes. Nat. Commun. 11:3114
    [Google Scholar]
  115. 115. 
    Zhang Y, Tsitkov S, Hess H. 2016. Proximity does not contribute to activity enhancement in the glucose oxidase-horseradish peroxidase cascade. Nat. Commun. 7:13982
    [Google Scholar]
  116. 116. 
    Zhang Z, Yang Y, Pincet F, Llaguno MC, Lin C. 2017. Placing and shaping liposomes with reconfigurable DNA nanocages. Nat. Chem. 9:653–59
    [Google Scholar]
  117. 117. 
    Zhou C, Yang Z, Liu D 2012. Reversible regulation of protein binding affinity by a DNA machine. J. Am. Chem. Soc. 134:1416–18
    [Google Scholar]
  118. 118. 
    Zhou L, Marras AE, Su H-J, Castro CE. 2015. Direct design of an energy landscape with bistable DNA origami mechanisms. Nano Lett 15:1815–21
    [Google Scholar]
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